Genes Controlling Neural Fate and Differentiation

  • Rebecca Matsas
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 429)

Abstract

All neural functions—from simple sensory responses and motor commands to elaborate cognitive behaviours—depend on the assembly of neural circuits, a process initiated during embryonic development. An early and fundamental step in this process is the generation of distinct classes of neurons at precise locations within a primitive neural epithelium (reviewed in Tanabe and Jessel, 1996). Over the past decade, many of the mechanisms that control the identity of specific neural cell types have been defined, in large part through the application of molecular genetics in invertebrate organisms such as Drosophila and Caenorhanditis elegans but also through cellular and biochemical approaches in vertebrates. Collectively, the study of these diverse systems has provided considerable insight into the relative contributions of environmental signaling and lineage restrictions in neural development and has revealed the identity of many of the extracellular signalling factors and intracellular proteins that direct cell fate. In this chapter we a) present a brief overview of recent progress made in defining positive and negative regulators of neurogenesis in vertebrates and their similarities with invertebrate organisms, b) discuss how genes regulating cell-cycle are also essential participants in neural differentiation and c) review recent data implicating neuron-specific markers in neuronal differentiation.

Keywords

Neuronal Differentiation Neural Differentiation Neural Precursor Xenopous Embryo bHLH Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aoki N., Yamaguchi-Aoki Y. and Ulrich A. (1996) The novel protein-tyrosine phosphatase PTP20 is a positive regulator of PCl2 cell neuronal differentiation. J. Biol. Chem. 271: 29422–29426.Google Scholar
  2. Artavanis-Tsaconas S., Matsuno K. and Fortini M. E. (1995) Notch signalling. Science 268: 225–232. Bain G., Ray W. J., Yao M. and Gottlieb D. I. (1994) Bioessays 16: 343–348.Google Scholar
  3. Brummendorf T., Wolff J.M., Frank R., and F.G. Rathjen (1989) Neural cell recognition molecule FI I: homology with fibronectin type Ill and immunoglobulin C domains. Neuron, 2: 1351–1361.PubMedCrossRefGoogle Scholar
  4. Brummendorf, T., and Rathjen. F. (1995) Cell adhesion molecules I: immunoglobulin superfamily. Protein Profile 2: 963–1108.PubMedGoogle Scholar
  5. Campos-Ortega J. A. (1996) Numb diverts notch pathway off the tramtrack. Neuron 17: 1–4.PubMedCrossRefGoogle Scholar
  6. Chan S. S., Zheng H., Su M. W., Wilk R., Killeen M. T., Hedgecock E. M. and Culotti J. G. (1996) UNC-40, a C. elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87: 187–195.PubMedCrossRefGoogle Scholar
  7. Chenn A. and McConnel S. K. (1995) Cleavage orientation and the asymmetric inheritance of Notch-1 immunoreactivity in mammalian neurogenesis. Cell 82: 631–641.PubMedCrossRefGoogle Scholar
  8. Chitnis A., Henrique D., Lewis J., Ish-Horowitz D. and Kintner C. (1995) Primary neurogenesis in Xenopous embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375: 761–766.PubMedCrossRefGoogle Scholar
  9. Chong J. A., Tapia-Ramirez J., Kim S., Toledo-Aral J., Zheng Y., Boutros M. C., Altshiller Y., Frohman M. A. Kraner S. D. and Mandel G. (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80: 949–957.Google Scholar
  10. Culotti J. G. and Kolodkin A. L. (1996) Functions of netrins and semaphorins in axon guidance. Curr. Opin. Neurobiol. 6: 81–88.Google Scholar
  11. Cunningham B. A., Hemperly J. J., Murray G. A., Prediger E. A., Brackenbury B. and Edelman G. M. (1987) Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236: 799–806.PubMedCrossRefGoogle Scholar
  12. Dehay C., Giroud P., Berland M. Smart I. and Kennedy H. (1993) Modulation of the cell cycle contributes to the parcellation of the primate visual cortex. Nature 366: 464–466.Google Scholar
  13. Doherty P, and Walsh, F. (1994) Signal transduction events underlaying neurite outgrowth stimulated by cell adhesion molecules. Curr. Opin. Neurobiol. 4: 49–55.Google Scholar
  14. Doherty P, and Walsh, F. (1996) CAM-FGF interaction: amodel for axonal growth. Mol. Cell. Neurosci., 8: 99–111.Google Scholar
  15. Ebens A. J., Garren H. Cheyette B. N. and Zipursky S. L. (1193) The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74: 15–27.Google Scholar
  16. Feany, M. B. and Buckley, K. M. (1993) The synaptic vesicle protein synaptotagmin promotes formation of filopodia in fibroblasts. Nature 364: 537–540.PubMedCrossRefGoogle Scholar
  17. Ferguson E. L. and Anderson K. V. (1992) decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71: 451–461.Google Scholar
  18. Ferreiro B., Skoglund P., Bailey A., Dorsky R. and Harris W. (1992) XASH-1, a Xenopous homolog of achaetescute: a proneural gene in anterior regions of the vertebrate CNS. Mech. Dev. 40: 25–36.Google Scholar
  19. Fields, D., and Itoh, K. (1996) Neural cell adhesion molecules in activity-dependent development and synaptic plasticity. Trends Neurosci. 19: 473–480.PubMedCrossRefGoogle Scholar
  20. Furley A.J., Morton S.B., Manalo D. Karagogeos D., Dodd J. and T.M. Jesse]] (1990) The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth promoting activity. Cell, 61: 157–170.Google Scholar
  21. Gao W. O., Heintz N. and Hatten M. E. (1991) Cerebellar granule cell neurogenesis is regulated by cell-cell interactions in vitro. Neuron 6: 705–715.PubMedCrossRefGoogle Scholar
  22. Gennarini, G., G. Cibelli, G. Rougon, M Mattei, G. and Goridis, C. (1989) The mouse neuronal cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to the chicken contactin. J. Cell Biol. 109: 775–788.PubMedCrossRefGoogle Scholar
  23. Godsave S. F. and Slack J. M. Single cell analysis of mesoderm formation in the Xenopous embryo. Development 111, 523–530.Google Scholar
  24. Green J. B. A. (1994) Roads to neuralness: embryonic neural induction as depression of a default state. Cell 77: 317–320.PubMedCrossRefGoogle Scholar
  25. Guillemot F. and Joyner A. L. (1993) Dynamic expression of the murine achaetc-scuce homologue Mash-1 in the developing nervous system. Mech. Dev. 42: 171–185.Google Scholar
  26. Guillemot F., Lo L. C., Johnson J. E., Auerbach A. Anderson D. J. and Joyner A. L. (1993) Mammalian achaetescute homolog-1 is required for early development of olfactory and autonomic neurons. Cell 75: 463–476.Google Scholar
  27. Heitzler P. and Simpson P. (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64: 1083–1092.PubMedCrossRefGoogle Scholar
  28. Hemmati-Brinvalou A. and Melton D. A. (1994) Inhibition ofactivin receptor signaling promotes neuralization in Xenopous. Cell 77: 273–281.CrossRefGoogle Scholar
  29. Hengartner M. O. and Horvitz H. R. (1994) C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bc1–2. Cell 76: 655–676.CrossRefGoogle Scholar
  30. Henrique D., Adam J., Myat A., Chitnis A., Lewis J. and Ish-Horowicz D. (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 375: 787–790.PubMedCrossRefGoogle Scholar
  31. Holley S. A., Jackson P. D., Sasai Y., Lu B., De Robertis E. M., Hoffmann F. M. and Ferguson E. L. (1995) A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and Iron/in. Nature 376: 249–253.PubMedCrossRefGoogle Scholar
  32. Jan Y. N. and Jan L. Y. (1993) HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell 75: 827–830.PubMedCrossRefGoogle Scholar
  33. Jan Y. N. and Jan L. Y. (1994) Genetic control of cell fate specification in the Drosophila peripheral nervous system. Ann. Rev. Genet. 28: 373–393.Google Scholar
  34. Janiak F., Leber B. and Andrews D. W. (1994) Assembly of 13cl-2 into microsomal and outer mitochondria) membranes. J. Biol. Chem. 269: 9842–9849.Google Scholar
  35. Jones L. S. (1996) Integrins: possible functions in the adult CNS. Trends Neurosci. 19: 68 72.Google Scholar
  36. Keino-Masu K., Masu M., Hinck L., Leonardo E. D., Chan S. S., Culotti J. G. and Tessier-Lavigne M. (1996) Deleted in Colorectal Cancer ( DCC) encodes a netrin receptor. Cell 87: 175–185Google Scholar
  37. Kraner S. D., Chong J. A., Tsay H. J. and Mandel G. (1992) Silencing the type II sodium channel gene: a model for neural specific gene regulation. Neuron 9: 37–44.PubMedCrossRefGoogle Scholar
  38. Kumagai-Tohda, C., Tohda, M. and Nomura. Y. (1993) Increas in formation and acetylcholine release by transfec- tion of growth-associated protein GAP-43 eDNA into NG108–15 cells. J. Neurochem. 61: 526–532.PubMedCrossRefGoogle Scholar
  39. LeClerc N., Kosik K. S., Cowan, N. Pienkowski, T. P. and Baas, P. W. (1993) Process formation in Sf9 cells induced by the expression of a microtubule-associated protein 2C-like construct. Proc. Natl. Acad. Sci. USA 90: 6223–6227.Google Scholar
  40. Lee J. E., Hollenberg S. M., Snider L., Turner D. L., Lipnick N and Weintraub H. (1995) Conversion of Xenopous ectoderm into neurons by NeuroD, a basic Helix-Loop-Helix protein. Science 268: 836–844.PubMedCrossRefGoogle Scholar
  41. Li L., Suzuki T., Mori N. and Greengard P. (1993) Identification of a functional silencer element involved in neuron-specific expression of the synapsin I gene. Proc. Natl. Acad. Sci. USA 90: 1460–1464.Google Scholar
  42. Ma Q., Kintner C. and Anderson D. J. (1996) Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87: 43–52.PubMedCrossRefGoogle Scholar
  43. Mamalaki A. Boutou E. Hurel C. Patsavoudi E. Tzartos S. and Matsas R. (1995) The BM88 antigen, a novel neuron-specific molecule, enhances the differentiation of mouse neuroblastoma cells. J. Biol. Chem. 270: 14201–14208.Google Scholar
  44. Martinou J. C., Dubois-Dauphin M., Staple J. K., Rodriguez L. Frankowski H., Missottcn M., Albertini P., Talabot D., Katsikas S., Piera C. and Huarte J. (1994) Overexpression of BCL-2 in transgenic mice protects neurons from naturally occuring cell death and experimental ischemia. Neuron 13: 1017–1030.PubMedCrossRefGoogle Scholar
  45. McConnel S. K. and Kaznowski C. E. (1991) Cell cycle dependence of laminar determination in developing cerebral cortex. Science 254: 282–285.CrossRefGoogle Scholar
  46. Moos M., Tacke R., Schere H., Teploe D., Fruh K. and Schachner M. (1988) Neural adhesion molecule LI as a member of the immunoglobulin superfamily with binding domains similar to fibronectin Nature 334: 701–703.Google Scholar
  47. Mori N., Schoenherr C., Vandenbergh D. J. and Anderson D. J. (1992) A common silencer element in the SC’G10 and type II Na` chanel genes binds a factor present in non-neuronal cells but not in neuronal cells. Neuron 9: 45–54.PubMedCrossRefGoogle Scholar
  48. Morton, A. J. and Buss, T. N. (1992) Accelerated differentiation in response to retinoic acid after retrovirally mediated gene transfer of GAP-43 into mouse neuroblastoma cells. Eur. J. Neurosci. 4: 910–916.Google Scholar
  49. Olson E. N. and Klein W. H. (1994) bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8: 1–8.Google Scholar
  50. Oppenheim R. W. (1991) Cell death during development of the nervous system. Ann. Rev. Neurosci. 14: 453–501.Google Scholar
  51. Patsavoudi E., Hurel, C. and Matsas, R. (1989) Neuron and myelin specific monoclonal antibodies recognizing cell surface antigens of the central and peripheral nervous system. Neuroscience 30: 463–478.PubMedCrossRefGoogle Scholar
  52. Patsavoudi E., Hurel C. and Matsas R. (1991) Purification and characterization of neuron-specific surface antigen defined by monoclonal antibody BM88. J. Neurochem. 56: 782–788.PubMedCrossRefGoogle Scholar
  53. Patsavoudi E., Merkouri E., Thomaidou D., Sandillon F., Alonso G. and Matsas, R. (1995) Characterization and localization of the BM88 antigen in the developing and adult rat brain. J. Neurosci. Res., 40: 506–518.Google Scholar
  54. Piccolo S., Sasai Y., Lu B. and De Robertis E.M. (1996) Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86: 589–598.PubMedCrossRefGoogle Scholar
  55. Raff M. C., Barres B. A., Burne J. F., Coles H. S., Ishizaki Y. and Jacobson M. D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262: 695–700.PubMedCrossRefGoogle Scholar
  56. Ranscht, B. (1988) Sequence of contactin, a 130 kD glycoprotein concentrated in areas of interneural contact, defines a new member of the Ig superfamily in the nervous system. J. Cell Biol. 104: 343–353.Google Scholar
  57. Ross E. M. (1996) Cell division and the nervous system: regulating the cell-cycle from neural differentiation to death. Trends Neurosci. 19: 62–68.PubMedCrossRefGoogle Scholar
  58. Sasai Y., Lu B., Steinbeisser H. and De Robertis E. M. (1995) Regulation of neural induction by the chordin and Bmp-4 antagonistic patterning signals in Xenopous. Nature 376: 333–336.PubMedCrossRefGoogle Scholar
  59. Schoenherr C. J. and Anderson D. J. (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267: 1360–1363.PubMedCrossRefGoogle Scholar
  60. Simpson P. (1995) Positive and negative regulators of neural fate. Neuron 15: 739–742.PubMedCrossRefGoogle Scholar
  61. Steller H. (1995) Mechanisms and genes of cellular suicide. Science 267: 1445–1449.PubMedCrossRefGoogle Scholar
  62. Tacheichi M. (1990) Cadherins: a molecular family important in selective cell-cell adhesion. Ann. Rev. Bioch. 59: 237–252.CrossRefGoogle Scholar
  63. Tanabe Y. and Jesse] T. M. (1996) Diversity and pattern in the developing spinal cord. Science 274: 115–1123.CrossRefGoogle Scholar
  64. Tessier-Lavigne M and Goodman C. (1996) The molecular biology of axon guidance. Science 274: 1123–1132.PubMedCrossRefGoogle Scholar
  65. Turner D. L. and Weintraub H. (1994) Expression ofachaete-scute homolog 3 in Xenopous embryos converts ectodermal cells to a neural fate. Genes Dev. 8: 1434–1447.PubMedCrossRefGoogle Scholar
  66. Waid D. K. and McLoon C. (1995) Immediate differentiation of ganglion cells following mitosis in the developing retina. Neuron 14: 117–124.PubMedCrossRefGoogle Scholar
  67. Weintraub H. (1993) The MyoD family and myogenesis: redundancy, networks and thresholds. Cell 75: 1241–1244.PubMedCrossRefGoogle Scholar
  68. Wilson P. A. and Hemmati-Brivanlou A. (1995) Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376: 331–333.PubMedCrossRefGoogle Scholar
  69. Yamashita H., ten-Dijke P., Huylebroeck D., Sampath T. K., Andries M., Smith J. C., Heldin C. H. and Miyazono K. (1995) Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130, 217–226.PubMedCrossRefGoogle Scholar
  70. Yuan J. and Horvitz H. R. (1992) The ceanorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 116: 309–320.PubMedGoogle Scholar
  71. Yuan J., Shaham S., Ledoux S., Ellis H. M. and Horvitz H. R. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 ß-converting enzyme. Cell 75: 641–652.PubMedCrossRefGoogle Scholar
  72. Zhao C. and Emmons S. W. (1995) A transcription factor controlling development of peripheral sense organs in C. elegans. Nature 373: 74–78.PubMedCrossRefGoogle Scholar
  73. Zhong W., Feder J. N., Jiang M. M., Jan L. Y. and Jan Y. N. (1996) Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17: 43–53.PubMedCrossRefGoogle Scholar
  74. Zimmerman K., Shih J., Bars J., Collazo A. and Anderson D. J. (1993) XASH-3, a novel Xenopous achaete-scute homolog, provides an early marker of planar neural induction and position along the medio-lateral axis of the neural plate. Development 119: 221–232.Google Scholar
  75. Zimmerman L. B., Jesus-Escobar J. M. and Harland R. M. (1996) The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599–606.PubMedCrossRefGoogle Scholar
  76. Zuber M. X., Goodman D. W., Karns L. R. and Fishman M. C. (1989) The neuronal growth-associated protein GAP-43 induces filopodia in non-neuronal cells. Science 244: 1193–1195.PubMedCrossRefGoogle Scholar
  77. Zuellig R., Rader C., Schroeder A., Kalousek F., vonBohlen and Halbach F., Osterwalder T., Inan C., Stoeckli E., Affolter U., Fritz A., Hafen, and P. Sonderegger (1992) The axonally secreted cell adhesion molecule, axonin-1: primary structure, Ig-and fibronectin type III-like domains, and glycosyl phosphatidylinositol anchorage. Eur. J. Biochem., 204: 453–463.Google Scholar

Copyright information

© Springer Science+Business Media New York 1997

Authors and Affiliations

  • Rebecca Matsas
    • 1
  1. 1.Department of BiochemistryHellenic Pasteur InstituteAthensGreece

Personalised recommendations